Reversible blockade of complex I or inhibition of PKCβ reduces activation and mitochondria translocation of p66Shcto preserve cardiac function after ischemia

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Yang, Meiying ^a   Stowe, David F ^a,b,c   Udoh, Kenechukwu B ^a   Heisner, James S ^a   Camara, Amadou K S ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b CLEMENT J ZABLOCKI VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c Marquette University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMOBARBITAL; HISPIDIN; PROTEIN KINASE C BETA; PROTEIN KINASE C BETA INHIBITOR; PROTEIN P66; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SERINE; UNCLASSIFIED DRUG; PROTEIN KINASE INHIBITOR; PROTEIN SHC;

ANIMAL TISSUE; ARTICLE; CELL LEVEL; CONTROLLED STUDY; CYTOSOL; ELECTRON TRANSPORT; ENZYME INHIBITION; GUINEA PIG; HEART FUNCTION; HEART INFARCTION SIZE; HEART MITOCHONDRION; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PROTECTION; MITOCHONDRION; NONHUMAN; OXIDATION REDUCTION STATE; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; ENZYME ACTIVATION; HEART; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PROTEIN TRANSPORT; REPERFUSION INJURY;

AMOBARBITAL; ANIMALS; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX I; ENZYME ACTIVATION; GUINEA PIGS; HEART; MITOCHONDRIA; MYOCARDIAL ISCHEMIA; PROTEIN KINASE C BETA; PROTEIN KINASE INHIBITORS; PROTEIN TRANSPORT; REPERFUSION INJURY; SHC SIGNALING ADAPTOR PROTEINS;

EID: 84914689001     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113534     Document Type: Article

References (48)

1. Camara AK, Lesnefsky EJ, Stowe DF (2010) Potential therapeutic benefits of strategies directed to mitochondria. Antioxid Redox Signal 13: 279-347.
2. Stowe DF, Camara AK (2009) Mitochondria reactive oxygen species production in excitable cells: Modulators of mitochondrial and cell function. Antioxid Redox Signal 11: 1373-1414.
3. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ (2003) Production of reactive oxygen species by mitochondria: Central role of complex III. J Biol Chem 278: 36027-36031.
4. St-Pierre J, Buckingham JA, Roebuck SJ, Brand MD (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 277: 44784-44790.
5. Quinlan CL, Orr AL, Perevoshchikova IV, Treberg JR, Ackrell BA, et al. (2012) Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions. J Biol Chem 287: 27255-27264.
6. Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122: 221-233.
7. Camara AK, Stowe DF (2014) ROS and cardiac ischemia and reperfusion injury. System Biology of Free Radicals and Anti-Oxidants Chapter 75: 1.
8. Camara AK, Bienengraeber M, Stowe DF (2011) Mitochondrial approaches to protect against cardiac ischemia and reperfusion injury. Front Physiol 2: 13.
9. Shc ablation: Up-regulation of anti-oxidant and anti-apoptotic proteins. J Hepatol 48: 422-432.
10. ShcA modulates tissue response to hindlimb ischemia. Circulation 109: 2917-2923.
11. Shc ablation demonstrate the crucial role of mitochondrial ROS formation in ischemia/ reperfusion injury. Biochim Biophys Acta 1787: 774-780.
12. Shc adaptor protein controls oxidative stress response and life span in mammals. Nature 402: 309-313.
13. Pinton P, Rimessi A, Marchi S, Orsini F, Migliaccio E, et al. (2007) Protein kinase C β and prolyl isomerase 1 regulate mitochondrial effects of the life-span determinant p66Shc. Science 315: 659-663.
14. Kong L, Andrassy M, Chang JS, Huang C, Asai T, et al. (2008) PKCβ modulates ischemia-reperfusion injury in the heart. Am J Physiol Heart Circ Physiol 294: H1862-70.
15. 2+ overload and ROS release. Cardiovasc Res 77: 406-415.
16. Chen Q, Lesnefsky EJ (2011) Blockade of electron transport during ischemia preserves bcl-2 and inhibits opening of the mitochondrial permeability transition pore. FEBS Lett 585: 921-926.
17. Chance B, Williams GR, Hollunger G (1963) Inhibition of electron and energy transfer in mitochondria. I. effects of amytal, thiopental, rotenone, progesterone, and methylene glycol. J Biol Chem 238: 418-431.
18. + Cardioplegia reduces superoxide emission during 2-hour global cold cardiac ischemia. J Cardiovasc Pharmacol Ther 17:93-101.
19. Camara AK, Riess ML, Kevin LG, Novalija E, Stowe DF (2004) Hypothermia augments reactive oxygen species detected in the guinea pig isolated perfused heart. Am J Physiol Heart Circ Physiol 286: H1289-99.
20. 2 radicals in intact hearts with ischemia and reperfusion. Am J Physiol Heart Circ Physiol 284: H566-74.
21. Novalija E, Varadarajan SG, Camara AK, An J, Chen Q, et al. (2002) Anesthetic preconditioning: Triggering role of reactive oxygen and nitrogen species in isolated hearts. Am J Physiol Heart Circ Physiol 283: H44-52.
22. +channels identified in guinea pig cardiac inner mitochondrial membrane. Biochim Biophys Acta 1828: 427-442.
23. + channel opening requires superoxide radical generation. Am J Physiol Heart Circ Physiol 290: H434-40.
24. 2+ overload, and changes in redox state. Am J Physiol Cell Physiol 292: C2021-31.
25. Aldakkak M, Stowe DF, Lesnefsky EJ, Heisner JS, Chen Q, et al. (2009) Modulation of mitochondrial bioenergetics in the isolated guinea pig beating heart by potassium and lidocaine cardioplegia: Implications for cardioprotection. J Cardiovasc Pharmacol 54: 298-309.
26. Riess ML, Camara AK, Chen Q, Novalija E, Rhodes SS, et al. (2002) Altered NADH and improved function by anesthetic and ischemic preconditioning in guinea pig intact hearts. Am J Physiol Heart Circ Physiol 283: H53-60.
27. Yang M, Camara AK, Wakim BT, Zhou Y, Gadicherla AK, et al. (2012) Tyrosine nitration of voltage-dependent anion channels in cardiac ischemia-reperfusion: Reduction by peroxynitrite scavenging. Biochim Biophys Acta 1817: 2049-2059.
28. 2+] increases during ATP/ADP antiport and ADP phosphorylation: Exploration of mechanisms. Biophys J 99: 997-1006.
29. + channels. Am J Physiol Heart Circ Physiol 293: H1400-7.
30. + channel opening. Am J Physiol Cell Physiol 298: C530-41.
31. Gadicherla AK, Stowe DF, Antholine WE, Yang M, Camara AK (2012) Damage to mitochondrial complex I during cardiac ischemia reperfusion injury is reduced indirectly by anti-anginal drug ranolazine. Biochim Biophys Acta 1817: 419-429.
32. Hiona A, Lee AS, Nagendran J, Xie X, Connolly AJ, et al. (2011) Pretreatment with angiotensin-converting enzyme inhibitor improves doxorubicin-induced cardiomyopathy via preservation of mitochondrial function. J Thorac Cardiovasc Surg 142: 396-403.e3.
33. Graham JM (2001) Purification of a crude mitochondrial fraction by density-gradient centrifugation. Curr Protoc Cell Biol Chapter 3: Unit 3.4.
34. Kanski J, Behring A, Pelling J, Schoneich C (2005) Proteomic identification of 3-nitrotyrosine-containing rat cardiac proteins: Effects of biological aging. Am J Physiol Heart Circ Physiol 288: H371-81.
35. Liu B, Tewari AK, Zhang L, Green-Church KB, Zweier JL, et al. (2009) Proteomic analysis of protein tyrosine nitration after ischemia reperfusion injury: Mitochondria as the major target. Biochim Biophys Acta 1794: 476-485.
36. Shi Y, Cosentino F, Camici GG, Akhmedov A, Vanhoutte PM, et al. (2011) Oxidized low-density lipoprotein activates p66Shc via lectin-like oxidized low-density lipoprotein receptor-1, protein kinase Cβ, and c-jun N-terminal kinase kinase in human endothelial cells. Arterioscler Thromb Vasc Biol 31: 2090-2097.
37. Gorenkova N, Robinson E, Grieve DJ, Galkin A (2013) Conformational change of mitochondrial complex I increases ROS sensitivity during ischemia. Antioxid Redox Signal.
38. Pagliaro P, Moro F, Tullio F, Perrelli MG, Penna C (2011) Cardioprotective pathways during reperfusion: Focus on redox signaling and other modalities of cell signaling. Antioxid Redox Signal 14: 833-850.
39. Piantadosi CA, Zhang J (1996) Mitochondrial generation of reactive oxygen species after brain ischemia in the rat. Stroke 27: 327-31; discussion 332.
40. Chen Q, Moghaddas S, Hoppel CL, Lesnefsky EJ (2008) Ischemic defects in the electron transport chain increase the production of reactive oxygen species from isolated rat heart mitochondria. Am J Physiol Cell Physiol 294: C460-6.
41. Sack MN (2006) Mitochondrial depolarization and the role of uncoupling proteins in ischemia tolerance. Cardiovasc Res 72: 210-219.
42. Veitch K, Hombroeckx A, Caucheteux D, Pouleur H, Hue L (1992) Global ischaemia induces a biphasic response of the mitochondrial respiratory chain. anoxic pre-perfusion protects against ischaemic damage. Biochem J 281 (Pt 3): 709-715.
43. Lesnefsky EJ, Moghaddas S, Tandler B, Kerner J, Hoppel CL (2001) Mitochondrial dysfunction in cardiac disease: Ischemia-reperfusion, aging, and heart failure. J Mol Cell Cardiol 33: 1065-1089.
44. Horgan DJ, Singer TP, Casida JE (1968) Studies on the respiratory chain-linked reduced nicotinamide adenine dinucleotide dehydrogenase. 13. binding sites of rotenone, piericidin A, and amytal in the respiratory chain. J Biol Chem 243: 834-843.
45. Spiegel HE, Wainio WW (1969) Some features of barbiturate interaction and inhibition of NADH-cytochrome C oxidoreductase in respiring systems. J Pharmacol Exp Ther 165: 23-29.
46. Shc in oxidative stress and apoptosis. Acta Naturae 2: 44-51.
47. i3 interaction. Cell Signal 22: 325-329.
48. Yang CP, Horwitz SB (2002) Distinct mechanisms of taxol-induced serine phosphorylation of the 66-kDa shc isoform in A549 and RAW 264.7 cells. Biochim Biophys Acta 1590: 76-83.